Tanya M. Smith

Earliest evidence of modern human life history in North African early Homo sapiens

Recent developmental studies demonstrate that early fossil hominins possessed shorter growth periods than living humans, implying disparate life histories. Analyses of incremental features in teeth provide an accurate means of assessing the age at death of developing dentitions, facilitating direct comparisons with fossil and modern humans. It is currently unknown when and where the prolonged modern human developmental condition originated. Here, an application of x-ray synchrotron microtomography reveals that an early Homo sapiens juvenile from Morocco dated at 160,000 years before present displays an equivalent degree of tooth development to modern European children at the same age. Crown formation times in the juveniles macrodont dentition are higher than modern human mean values, whereas root development is accelerated relative to modern humans but is less than living apes and some fossil hominins. The juvenile from Jebel Irhoud is currently the oldest-known member of Homo with a developmental pattern (degree of eruption, developmental stage, and crown formation time) that is more similar to modern H. sapiens than to earlier members of Homo. This study also underscores the continuing importance of North Africa for understanding the origins of human anatomical and behavioral modernity. Corresponding biological and cultural changes may have appeared relatively late in the course of human evolution.

Dental evidence for ontogenetic differences between modern humans and Neanderthals

Humans have an unusual life history, with an early weaning age, long childhood, late first reproduction, short interbirth intervals, and long lifespan. In contrast, great apes wean later, reproduce earlier, and have longer intervals between births. Despite 80 y of speculation, the origins of these developmental patterns in Homo sapiens remain unknown. Because they record daily growth during formation, teeth provide important insights, revealing that australopithecines and early Homo had more rapid ontogenies than recent humans. Dental development in later Homo species has been intensely debated, most notably the issue of whether Neanderthals and H. sapiens differ. Here we apply synchrotron virtual histology to a geographically and temporally diverse sample of Middle Paleolithic juveniles, including Neanderthals, to assess tooth formation and calculate age at death from dental microstructure. We find that most Neanderthal tooth crowns grew more rapidly than modern human teeth, resulting in significantly faster dental maturation. In contrast, Middle Paleolithic H. sapiens juveniles show greater similarity to recent humans. These findings are consistent with recent cranial and molecular evidence for subtle developmental differences between Neanderthals and H. sapiens. When compared with earlier hominin taxa, both Neanderthals and H. sapiens have extended the duration of dental development. This period of dental immaturity is particularly prolonged in modern humans.

Rapid dental development in a Middle Paleolithic Belgian Neanderthal

The evolution of life history (pace of growth and reproduction) was crucial to ancient hominin adaptations. The study of dental development facilitates assessment of growth and development in fossil hominins with greater precision than other skeletal analyses. During tooth formation, biological rhythms manifest in enamel and dentine, creating a permanent record of growth rate and duration. Quantification of these internal and external incremental features yields developmental benchmarks, including ages at crown completion, tooth eruption, and root completion. Molar eruption is correlated with other aspects of life history. Recent evidence for developmental differences between modern humans and Neanderthals remains ambiguous. By measuring tooth formation in the entire dentition of a juvenile Neanderthal from Scladina, Belgium, we show that most teeth formed over a shorter time than in modern humans and that dental initiation and eruption were relatively advanced. By registering manifestations of stress across the dentition, we are able to present a precise chronology of Neanderthal dental development that differs from modern humans. At 8 years of age at death, this juvenile displays a degree of development comparable with modern human children who are several years older. We suggest that age at death in juvenile Neanderthals should not be assessed by comparison with modern human standards, particularly those derived from populations of European origin. Moreover, evidence from the Scladina juvenile and other similarly aged hominins suggests that a prolonged childhood and slow life history are unique to Homo sapiens.

Dental tissue proportions and enamel thickness in Neandertal and modern human molars.

The thickness of dental enamel is often discussed in paleoanthropological literature, particularly with regard to differences in growth, health, and diet between Neandertals and modern humans. Paleoanthropologists employ enamel thickness in paleodietary and taxonomic studies regarding earlier hominins, but variation in enamel thickness within the genus Homo has not been thoroughly explored despite its potential to discriminate species and its relevance to studies of growth and development. Radiographic two-dimensional studies indicate that Neandertal molar enamel is thin relative to the thick enamel of modern humans, although such methods have limited accuracy. Here we show that, measured via accurate high-resolution microtomographic imaging, Neandertal molar enamel is absolutely and relatively thinner than modern human enamel at most molar positions. However, this difference relates to the ratio of coronal dentine volume to total crown volume, rather than the quantity of enamel per se. The absolute volume of Neandertal molar enamel is similar to that of modern humans, but Neandertal enamel is deposited over a larger volume of coronal dentine, resulting in lower average (and relative) enamel thickness values. Sample sizes do not permit rigorous intragroup comparisons, but Neandertal molar tissue proportions evince less variation than the modern human sample. Differences in three- and two-dimensional enamel thickness data describing Neandertal molars may be explained by dimensional reduction. Although molar tissue proportions distinguish Neanderthals from recent Homo sapiens, additional study is necessary to assess trends in tissue proportions in the genus Homo throughout the Pleistocene.

Enamel thickness, microstructure and development in Afropithecus turkanensis.

Afropithecus turkanensis, a 17-17.5 million year old large-bodied hominoid from Kenya, has previously been reported to be the oldest known thick-enamelled Miocene ape. Most investigations of enamel thickness in Miocene apes have been limited to opportunistic or destructive studies of small samples. Recently, more comprehensive studies of enamel thickness and microstructure in Proconsul, Lufengpithecus, and Dryopithecus, as well as extant apes and fossil humans, have provided information on rates and patterns of dental development, including crown formation time, and have begun to provide a comparative context for interpretation of the evolution of these characters throughout the past 20 million years of hominoid evolution. In this study, enamel thickness and aspects of the enamel microstructure in two A. turkanensis second molars were quantified and provide insight into rates of enamel apposition, numbers of cells actively secreting enamel, and the time required to form regions of the crown. The average value for relative enamel thickness in the two molars is 21.4, which is a lower value than a previous analysis of this species, but which is still relatively thick compared to extant apes. This value is similar to those of several Miocene hominoids, a fossil hominid, and modern humans. Certain aspects of the enamel microstructure are similar to Proconsul nyanzae, Dryopithecus laietanus, Lufengpithecus lufengensis, Graecopithecus freybergi and Pongo pygmaeus, while other features differ from extant and fossil hominoids. Crown formation times for the two teeth are 2.4-2.6 years and 2.9-3.1 years respectively. These times are similar to a number of extant and fossil hominoids, some of which appear to show additional developmental similarities, including thick enamel. Although thick enamel may be formed through several developmental pathways, most Miocene hominoids and fossil hominids with relatively thick enamel are characterized by a relatively long period of cuspal enamel formation and a rapid rate of enamel secretion throughout the whole cusp, but a shorter total crown formation time than thinner-enamelled extant apes.

Barium distributions in teeth reveal early-life dietary transitions in primates

Early-life dietary transitions reflect fundamental aspects of primate evolution and are important determinants of health in contemporary human populations. Weaning is critical to developmental and reproductive rates; early weaning can have detrimental health effects but enables shorter inter-birth intervals, which influences population growth. Uncovering early-life dietary history in fossils is hampered by the absence of prospectively validated biomarkers that are not modified during fossilization. Here we show that large dietary shifts in early life manifest as compositional variations in dental tissues. Teeth from human children and captive macaques, with prospectively recorded diet histories, demonstrate that barium (Ba) distributions accurately reflect dietary transitions from the introduction of mother’s milk through the weaning process. We also document dietary transitions in a Middle Palaeolithic juvenile Neanderthal, which shows a pattern of exclusive breastfeeding for seven months, followed by seven months of supplementation. After this point, Ba levels in enamel returned to baseline prenatal levels, indicating an abrupt cessation of breastfeeding at 1.2 years of age. Integration of Ba spatial distributions and histological mapping of tooth formation enables novel studies of the evolution of human life history, dietary ontogeny in wild primates, and human health investigations through accurate reconstructions of breastfeeding history.

Age at first molar emergence in early Miocene Afropithecus turkanensis and life-history evolution in the Hominoidea

Among primates, age at first molar emergence is correlated with a variety of life history traits. Age at first molar emergence can therefore be used to broadly infer the life histories of fossil primate species. One method of determining age at first molar emergence is to determine the age at death of fossil individuals that were in the process of erupting their first molars. This was done for an infant partial mandible of Afropithecus turkanensis (KNM-MO 26) from the approximately 17.5 Ma site of Moruorot in Kenya. A range of estimates of age at death was calculated for this individual using the permanent lateral incisor germ preserved in its crypt, by combining the number and periodicity of lateral enamel perikymata with estimates of the duration of cuspal enamel formation and the duration of the postnatal delay in the inception of crown mineralization. Perikymata periodicity was determined using daily cross striations between adjacent Retzius lines in thin sections of two A. turkanensis molars from the nearby site of Kalodirr. Based on the position of the KNM-MO 26 M(1)in relation to the mandibular alveolar margin, it had not yet undergone gingival emergence. The projected time to gingival emergence was estimated based on radiographic studies of M(1)eruption in extant baboons and chimpanzees. The estimates of age at M(1)emergence in KNM-MO 26 range from 28.2 to 43.5 months, using minimum and average values from extant great apes and humans for the estimated growth parameters. Even the absolute minimum value is well outside the ranges of extant large Old World monkeys for which there are data (12.5 to <25 months), but is within the range of chimpanzees (25.7 to 48.0 months). It is inferred, therefore, that A. turkanensis had a life history profile broadly like that of Pan. This is additional evidence to that provided by Sivapithecus parvada (Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations, 1997, 173) that the prolonged life histories characteristic of extant apes were achieved early in the evolutionary history of the group. However, it is unclear at present whether life-history prolongation in apes represents the primitive catarrhine pace of life history extended through phyletic increase in body mass, or whether it is derived with respect to a primitive, size-adjusted life history that was broadly intermediate between those of extant hominoids and cercopithecoids. Life history evolution in primates as a whole may have occurred largely through a series of grade-shifts, with the establishment of fundamental life-history profiles early in the histories of major higher taxa. These may have included shifts that were largely body mass dependent, as well as those that occurred in the absence of significant changes in body mass.

Experimental determination of the periodicity of incremental features in enamel

Vital labelling of hard tissues was used to examine the periodicity of features of dental enamel microstructure. Fluorescent labels were administered pre‐ and postnatally to developing macaques (Macaca nemestrina), which were identified histologically in dentine and related to accentuated lines in enamel, allowing for counts of features within known‐period intervals. This study demonstrates that cross‐striations represent a daily rhythm in enamel secretion, and suggests that intradian lines are the result of a similar 12‐h rhythm. Retzius lines were found to have a regular periodicity within individual dentitions, and laminations appear to represent a daily rhythm that also shows 12‐h subdivisions. The inclusion of intradian lines and laminations represents the first empirical evidence for their periodicities in primates; these features frequently complicate precise measurements of secretion rate and Retzius line periodicity, which are necessary for determination of crown formation time. The biological basis of incremental feature formation is not completely understood; long‐period features may result from interactions between short‐period rhythms, although this does not explain the known range of Retzius line periodicities within humans or among primates. Studies of the genetic, neurological and hormonal basis of incremental feature formation are needed to provide more insight into their physiological and structural basis.

Three-dimensional molar enamel distribution and thickness in Australopithecus and Paranthropus

Thick molar enamel is among the few diagnostic characters of hominins which are measurable in fossil specimens. Despite a long history of study and characterization of Paranthropus molars as relatively ‘hyper-thick’, only a few tooth fragments and controlled planes of section (designed to be proxies of whole-crown thickness) have been measured. Here, we measure molar enamel thickness in Australopithecus africanus and Paranthropus robustus using accurate microtomographic methods, recording the whole-crown distribution of enamel. Both taxa have relatively thick enamel, but are thinner than previously characterized based on two-dimensional measurements. Three-dimensional measurements show that P. robustus enamel is not hyper-thick, and A. africanus enamel is relatively thinner than that of recent humans. Interspecific differences in the whole-crown distribution of enamel thickness influence cross-sectional measurements such that enamel thickness is exaggerated in two-dimensional sections of A. africanus and P. robustus molars. As such, two-dimensional enamel thickness measurements in australopiths are not reliable proxies for the three-dimensional data they are meant to represent. The three-dimensional distribution of enamel thickness shows different patterns among species, and is more useful for the interpretation of functional adaptations than single summary measures of enamel thickness.

The accuracy of histological assessments of dental development and age at death

Histological analyses of dental development have been conducted for several decades despite few studies assessing the accuracy of such methods. Using known‐period incremental features, the crown formation time and age at death of five pig‐tailed macaques (Macaca nemestrina) were estimated with standard histological techniques and compared with known ages. Estimates of age at death ranged from 8.6% underestimations to 15.0% overestimations, with an average 3.5% overestimate and a 7.2% average absolute difference. Several sources of error were identified relating to preparation quality and section obliquity. These results demonstrate that histological analyses of dental development involving counts and measurements of short‐ and long‐period incremental features may yield accurate estimates, particularly in well‐prepared material. Values from oblique sections (or most naturally fractured teeth) should be regarded with caution, as obliquity leads to inflated cuspal enamel formation time and underestimated imbricational formation time. Additionally, Shelliss formula for extension rate and crown formation time estimation was tested, which significantly overestimated crown formation time due to underestimated extension rate. It is suggested that Shellis’ method should not be applied to teeth with short, rapid periods of development, and further study is necessary to validate this application in other material.